Long-Term Persistence of Donor Alveolar Macrophages in Human Lung Transplant Recipients That Influences Donor-Specific Immune Responses

American Journal of Transplantation

Volumn 16, Issue 8, 2016, Pages 2300-2311

  Nayak, D K ^a,b   Zhou, F ^b   Xu, M ^b   Huang, J ^c   Tsuji, M ^c   Hachem, R ^b   Mohanakumar, T ^a,b  

^a ST JOSEPH'S HOSPITAL AND MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

alloantibody; animal model; basic (laboratory) research science; bronchiolitis obliterans (BOS); clinical research practice; immunosuppression immune modulation; lung (allograft) function dysfunction; lung transplantation pulmonology; macrophage monocyte biology

Indexed keywords

COLLAGEN TYPE 5; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA A2 ANTIGEN; HLA A3 ANTIGEN; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE TRANSFER; ALLOIMMUNITY; ANIMAL CELL; ARTICLE; CELLULAR IMMUNITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONNECTIVE TISSUE DISEASE; CONTROLLED STUDY; CYSTIC FIBROSIS; FIBROSING ALVEOLITIS; GRAFT RECIPIENT; HISTOCOMPATIBILITY; HUMAN; LUNG ALVEOLUS MACROPHAGE; LUNG GRAFT REJECTION; LUNG LAVAGE; LUNG TRANSPLANTATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; STEADY STATE;

EID: 84978924120     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13819     Document Type: Article

References (63)

1. Davies LC, Jenkins SJ, Allen JE, Taylor PR. Tissue-resident macrophages. Nat Immunol 2013; 14: 986–995.
2. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011; 11: 723–737.
3. Kopf M, Schneider C, Nobs SP. The development and function of lung-resident macrophages and dendritic cells. Nat Immunol 2015; 16: 36–44.
4. Guilliams M, De Kleer I, Henri S, et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med 2013; 210: 1977–1992.
5. Stone KC, Mercer RR, Gehr P, Stockstill B, Crapo JD. Allometric relationships of cell numbers and size in the mammalian lung. Am J Respir Cell Mol Biol 1992; 6: 235–243.
6. Westphalen K, Gusarova GA, Islam MN, et al. Sessile alveolar macrophages communicate with alveolar epithelium to modulate immunity. Nature 2014; 506: 503–506.
7. Schneider C, Nobs SP, Heer AK, et al. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog 2014; 10: e1004053.
8. Happle C, Lachmann N, Skuljec J, et al. Pulmonary transplantation of macrophage progenitors as effective and long-lasting therapy for hereditary pulmonary alveolar proteinosis. Sci Transl Med 2014; 6: 250ra113.
9. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003; 19: 71–82.
10. van Furth R, Cohn ZA. The origin and kinetics of mononuclear phagocytes. J Exp Med 1968; 128: 415–435.
11. Gordon SB, Read RC. Macrophage defences against respiratory tract infections. Br Med Bull 2002; 61: 45–61.
12. Sieweke MH, Allen JE. Beyond stem cells: Self-renewal of differentiated macrophages. Science 2013; 342: 1242974-1-7.
13. Perdiguero GE, Klapproth K, Schulz C, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 2015; 518: 547–551.
14. Hoeffel G, Chen J, Lavin Y, et al. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 2015; 42: 665–678.
15. Schneider C, Nobs SP, Kurrer M, Rehrauer H, Thiele C, Kopf M. Induction of the nuclear receptor PPAR-gamma by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat Immunol 2014; 15: 1026–1037.
16. Schulz C, Gomez Perdiguero E, Chorro L, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012; 336: 86–90.
17. Yamane T, Kunisada T, Yamazaki H, Era T, Nakano T, Hayashi SI. Development of osteoclasts from embryonic stem cells through a pathway that is c-fms but not c-kit dependent. Blood 1997; 90: 3516–3523.
18. Murphy J, Summer R, Wilson AA, Kotton DN, Fine A. The prolonged life-span of alveolar macrophages. Am J Respir Cell Mol Biol 2008; 38: 380–385.
19. Bharat A, Saini D, Steward N, et al. Antibodies to self-antigens predispose to primary lung allograft dysfunction and chronic rejection. Ann Thorac Surg 2010; 90: 1094–1101.
20. Girnita AL, Duquesnoy R, Yousem SA, et al. HLA-specific antibodies are risk factors for lymphocytic bronchiolitis and chronic lung allograft dysfunction. Am J Transplant 2005; 5: 131–138.
21. Saini D, Weber J, Ramachandran S, et al. Alloimmunity-induced autoimmunity as a potential mechanism in the pathogenesis of chronic rejection of human lung allografts. J Heart Lung Transplant 2011; 30: 624–631.
22. Snyder LD, Wang Z, Chen DF, et al. Implications for human leukocyte antigen antibodies after lung transplantation: A 10-year experience in 441 patients. Chest 2013; 144: 226–233.
23. Baskaran G, Tiriveedhi V, Ramachandran S, et al. Efficacy of extracorporeal photopheresis in clearance of antibodies to donor-specific and lung-specific antigens in lung transplant recipients. J Heart Lung Transplant 2014; 33: 950–956.
24. Hachem RR, Yusen RD, Meyers BF, et al. Anti-human leukocyte antigen antibodies and preemptive antibody-directed therapy after lung transplantation. J Heart Lung Transplant 2010; 29: 973–980.
25. Ius F, Sommer W, Tudorache I, et al. Preemptive treatment with therapeutic plasma exchange and rituximab for early donor-specific antibodies after lung transplantation. J Heart Lung Transplant 2015; 34: 50–58.
26. Tinckam KJ, Keshavjee S, Chaparro C, et al. Survival in sensitized lung transplant recipients with perioperative desensitization. Am J Transplant 2015; 15: 417–426.
27. Huang J, Li X, Kohno K, et al. Generation of tissue-specific H-2Kd transgenic mice for the study of K(d)-restricted malaria epitope-specific CD8 + T-cell responses in vivo. J Immunol Methods 2013; 387: 254–261.
28. Fukami NRS, Saini D, Walter M, Chapman W, Patterson GA, Mohanakumar T. Antibodies to MHC class I induce autoimmunity: Role in the pathogenesis of chronic rejection. J Immunol 2009; 182: 309–318.
29. Hachem RR, Tiriveedhi V, Patterson GA, Aloush A, Trulock EP, Mohanakumar T. Antibodies to K-alpha 1 tubulin and collagen V are associated with chronic rejection after lung transplantation. Am J Transplant 2012; 12: 2164–2171.
30. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol 2013; 49: 503–510.
31. Yu YA, Hotten DF, Malakhau Y, et al. Flow cytometric analysis of myeloid cells in human blood, bronchoalveolar lavage, and lung tissues. Am J Respir Cell Mol Biol 2016; 54: 13–24.
32. Bharat A, Bhorade SM, Morales-Nebreda L, et al. Flow cytometry reveals similarities between lung macrophages in humans and mice. Am J Respir Cell Mol Biol 2016; 54: 147–149.
33. Fukami N, Ramachandran S, Saini D, et al. Antibodies to MHC class I induce autoimmunity: Role in the pathogenesis of chronic rejection. J Immunol 2009; 182: 309–318.
34. Takenaka M, Tiriveedhi V, Subramanian V, Hoshinaga K, Patterson AG, Mohanakumar T. Antibodies to MHC class II molecules induce autoimmunity: Critical role for macrophages in the immunopathogenesis of obliterative airway disease. PLoS ONE 2012; 7: e42370.
35. Kotloff RM, Thabut G. Lung transplantation. Am J Respir Crit Care Med 2011; 184: 159–171.
36. Jaramillo A, Smith MA, Phelan D, et al. Development of ELISA-detected anti-HLA antibodies precedes the development of bronchiolitis obliterans syndrome and correlates with progressive decline in pulmonary function after lung transplantation. Transplantation 1999; 67: 1155–1161.
37. Palmer SM, Davis RD, Hadjiliadis D, et al. Development of an antibody specific to major histocompatibility antigens detectable by flow cytometry after lung transplant is associated with bronchiolitis obliterans syndrome. Transplantation 2002; 74: 799–804.
38. Hayes D Jr, Black SM, Tobias JD, et al. Influence of human leukocyte antigen mismatching on bronchiolitis obliterans syndrome in lung transplantation. J Heart Lung Transplant 2016; 35: 186–194.
39. Judson MA, Sahn SA, Hahn AB. Origin of pleural cells after lung transplantation: From donor or recipient? Chest 1997; 112: 426–429.
40. Kjellström C, Ichimura K, Chen XJ, Riise GC, Collins VP. The origin of alveolar macrophages in the transplanted lung: A longitudinal microsatellite-based study of donor and recipient DNA. Transplantation 2000; 69: 1984–1986.
41. Kleeberger W, Rothamel T, Glockner S, Flemming P, Lehmann U, Kreipe H. High frequency of epithelial chimerism in liver transplants demonstrated by microdissection and STR-analysis. Hepatology 2002; 35: 110–116.
42. Kleeberger W, Versmold A, Rothamel T, et al. Increased chimerism of bronchial and alveolar epithelium in human lung allografts undergoing chronic injury. Am J Pathol 2003; 162: 1487–1494.
43. Lagaaij EL, Cramer-Knijnenburg GF, van Kemenade FJ, van Es LA, Bruijn JA, van Krieken JH. Endothelial cell chimerism after renal transplantation and vascular rejection. Lancet 2001; 357: 33–37.
44. Nakata K, Gotoh H, Watanabe J, et al. Augmented proliferation of human alveolar macrophages after allogeneic bone marrow transplantation. Blood 1999; 93: 667–673.
45. Quaini F, Urbanek K, Beltrami AP, et al. Chimerism of the transplanted heart. N Eng J Med 2002; 346: 5–15.
46. Rothmeier C, Roux E, Spiliopoulos A, Gerbase M, Nicod LP. Early chimerism of macrophages and lymphocytes in lung transplant recipients is predictive of graft tolerance. Transplantation 2001; 71: 1329–1333.
47. MacLean JA, Xia W, Pinto CE, Zhao L, Liu HW, Kradin RL. Sequestration of inhaled particulate antigens by lung phagocytes: A mechanism for the effective inhibition of pulmonary cell-mediated immunity. Am J Pathol 1996; 148: 657–666.
48. Kennedy DW, Abkowitz JL. Kinetics of central nervous system microglial and macrophage engraftment: Analysis using a transgenic bone marrow transplantation model. Blood 1997; 90: 986–993.
49. Strauss-Ayali D, Conrad SM, Mosser DM. Monocyte subpopulations and their differentiation patterns during infection. J Leukoc Biol 2007; 82: 244–252.
50. Tomlinson GS, Booth H, Petit SJ, et al. Adherent human alveolar macrophages exhibit a transient pro-inflammatory profile that confounds responses to innate immune stimulation. PLoS ONE 2012; 7: e40348.
51. Noppen M. Normal volume and cellular contents of pleural fluid. Paediatr Respir Rev 2004; 5(Suppl A): S201–S203.
52. Hoeffel G, Ginhoux F. Ontogeny of tissue-resident macrophages. Front Immunol 2015; 6: 486.
53. Everhart MB, Han W, Parman KS, et al. Intratracheal administration of liposomal clodronate accelerates alveolar macrophage reconstitution following fetal liver transplantation. J Leukoc Biol 2005; 77: 173–180.
54. Cai Y, Sugimoto C, Arainga M, Alvarez X, Didier ES, Kuroda MJ. In vivo characterization of alveolar and interstitial lung macrophages in rhesus macaques: Implications for understanding lung disease in humans. J Immunol 2014; 192: 2821–2829.
55. Nakamura T, Abu-Dahab R, Menger MD, et al. Depletion of alveolar macrophages by clodronate-liposomes aggravates ischemia-reperfusion injury of the lung. J Heart Lung Transplant 2005; 24: 38–45.
56. Ghoneim HE, Thomas PG, McCullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 2013; 191: 1250–1259.
57. Maus UA, Janzen S, Wall G, et al. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. Am J Respir Cell Mol Biol 2006; 35: 227–235.
58. Zhang X, Rozengurt E, Reed EF. HLA class I molecules partner with integrin beta4 to stimulate endothelial cell proliferation and migration. Sci Signal 2010; 3: ra85.
59. Hartwig SM, Holman KM, Varga SM. Depletion of alveolar macrophages ameliorates virus-induced disease following a pulmonary coronavirus infection. PLoS ONE 2014; 9: e90720.
60. Benoit A, Huang Y, Proctor J, Rowden G, Anderson R. Effects of alveolar macrophage depletion on liposomal vaccine protection against respiratory syncytial virus (RSV). Clin Exp Immunol 2006; 145: 147–154.
61. Macdonald DC, Singh H, Whelan MA, et al. Harnessing alveolar macrophages for sustained mucosal T-cell recall confers long-term protection to mice against lethal influenza challenge without clinical disease. Mucosal Immunol 2014; 7: 89–100.
62. Heidler KM, Baker K, Woods K, et al. Instillation of allogeneic lung antigen-presenting cells deficient in expression of major histocompatibility complex class I or II antigens have differential effects on local cellular and humoral immunity and on pathology in recipient murine lungs. Am J Respir Cell Mol Biol 2000; 23: 499–505.
63. Wilkes DS, Heidler KM, Bowen LK, et al. Allogeneic bronchoalveolar lavage cells induce the histology of acute lung allograft rejection, and deposition of IgG2a in recipient murine lungs. J Immunol 1995; 155: 2775–2783.